Alternative Computational Protocols for Supercharging Protein Surfaces for Reversible Unfolding and Retention of Stability

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Der, Bryan S ^a   Kluwe, Christien ^b   Miklos, Aleksandr E ^b   Jacak, Ron ^a   Lyskov, Sergey ^c   Gray, Jeffrey J ^c   Georgiou, George ^b   Ellington, Andrew D ^b   Kuhlman, Brian ^a,d  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c Johns Hopkins University   (United States)

^d UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ARTICLE; AUTOMATION; CALCULATION; CONTROLLED STUDY; ENERGY; EXPERIMENTAL STUDY; MUTATION; PROTEIN ENGINEERING; PROTEIN EXPRESSION; PROTEIN REFOLDING; PROTEIN STABILITY; PROTEIN SUPERCHARGING; PROTEIN UNFOLDING; SURFACE PROPERTY;

AMINO ACID SEQUENCE; AMINO ACIDS; ANIMALS; CNIDARIA; GREEN FLUORESCENT PROTEINS; HYDROGEN BONDING; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN CONFORMATION; PROTEIN ENGINEERING; PROTEIN STABILITY; PROTEIN UNFOLDING; SOFTWARE; STATIC ELECTRICITY; THERMODYNAMICS;

EID: 84878525763     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064363     Document Type: Article

References (61)

1. Fields GB, Alonso DOV, Stigter D, Dill KA, (1992) Theory for the Aggregation of Proteins and Copolymers. Journal of Physical Chemistry 96: 3974-3981.
2. Fink AL, (1998) Protein aggregation: folding aggregates, inclusion bodies and amyloid. Folding & Design 3: R9-R23.
3. Defelippis MR, Alter LA, Pekar AH, Havel HA, Brems DN, (1993) Evidence for a Self-Associating Equilibrium Intermediate during Folding of Human Growth-Hormone. Biochemistry 32: 1555-1562.
4. London J, Skrzynia C, Goldberg ME, (1974) Renaturation of Escherichia-Coli Tryptophanase after Exposure to 8 M Urea- Evidence for Existence of Nucleation Centers. European Journal of Biochemistry 47: 409-415.
5. Speed MA, Wang DIC, King J, (1996) Specific aggregation of partially folded polypeptide chains: The molecular basis of inclusion body composition. Nature Biotechnology 14: 1283-1287.
6. Speed MA, Wang DIC, King J, (1995) Multimeric Intermediates in the Pathway to the Aggregated Inclusion-Body State for P22 Tailspike Polypeptide-Chains. Protein Science 4: 900-908.
7. Goldberg ME, Rudolph R, Jaenicke R, (1991) A Kinetic-Study of the Competition between Renaturation and Aggregation during the Refolding of Denatured Reduced Egg-White Lysozyme. Biochemistry 30: 2790-2797.
8. Chiti F, Calamai M, Taddei N, Stefani M, Ramponi G, et al. (2002) Studies of the aggregation of mutant proteins in vitro provide insights into the genetics of amyloid diseases. Proceedings of the National Academy of Sciences of the United States of America 99: 16419-16426.
9. Zbilut JP, Mitchell JC, Giuliani A, Colosimo A, Marwan N, et al. (2004) Singular hydrophobicity patterns and net charge: a mesoscopic principle for protein aggregation/folding. Physica a-Statistical Mechanics and Its Applications 343: 348-358.
10. Frokjaer S, Otzen DE, (2005) Protein drug stability: A formulation challenge. Nature Reviews Drug Discovery 4: 298-306.
11. Wang W, (2005) Protein aggregation and its inhibition in biopharmaceutics. International Journal of Pharmaceutics 289: 1-30.
12. Dasnoy S, Dezutter N, Lemoine D, Le Bras V, Preat V, (2011) High-Throughput Screening of Excipients Intended to Prevent Antigen Aggregation at Air-Liquid Interface. Pharmaceutical Research 28: 1591-1605.
13. Kamerzell TJ, Esfandiary R, Joshi SB, Middaugh CR, Volkin DB, (2011) Protein-excipient interactions: Mechanisms and biophysical characterization applied to protein formulation development. Advanced Drug Delivery Reviews 63: 1118-1159.
14. Fowler SB, Poon S, Muff R, Chiti F, Dobson CM, et al. (2005) Rational design of aggregation-resistant bioactive peptides: Reengineering human calcitonin. Proceedings of the National Academy of Sciences of the United States of America 102: 10105-10110.
15. Mitraki A, King J, (1989) Protein Folding Intermediates and Inclusion Body Formation. Nature Biotechnology 7: 690-697.
16. Simeonov P, Berger-Hoffmann R, Hoffmann R, Strater N, Zuchner T, (2011) Surface supercharged human enteropeptidase light chain shows improved solubility and refolding yield. Protein Eng Des Sel 24: 261-268.
17. Simeonov P, Zahn M, Strater N, Zuchner T (2012) Crystal structure of a supercharged variant of the human enteropeptidase light chain. Proteins.
18. Ramm K, Gehrig P, Pluckthun A, (1999) Removal of the conserved disulfide bridges from the scFv fragment of an antibody: Effects on folding kinetics and aggregation. Journal of Molecular Biology 290: 535-546.
19. Dong AC, Prestrelski SJ, Allison SD, Carpenter JF, (1995) Infrared Spectroscopic Studies of Lyophilization-Induced and Temperature-Induced Protein Aggregation. Journal of Pharmaceutical Sciences 84: 415-424.
20. Miklos AE, Kluwe C, Der BS, Pai S, Sircar A, et al. (2012) Structure-based design of supercharged, highly thermoresistant antibodies. Chem Biol 19: 449-455.
21. Frankel AD, Pabo CO, (1988) Cellular Uptake of the Tat Protein from Human Immunodeficiency Virus. Cell 55: 1189-1193.
22. Fuchs SM, Raines RT, (2007) Arginine grafting to endow cell permeability. Acs Chemical Biology 2: 167-170.
23. Glukhov E, Burrows LL, Deber CM, (2008) Membrane interactions of designed cationic antimicrobial peptides: The two thresholds. Biopolymers 89: 360-371.
24. Heitz F, Morris MC, Divita G, (2009) Twenty years of cell-penetrating peptides: from molecular mechanisms to therapeutics. Br J Pharmacol 157: 195-206.
25. Cronican JJ, Beier KT, Davis TN, Tseng JC, Li WD, et al. (2011) A Class of Human Proteins that Deliver Functional Proteins into Mammalian Cells In Vitro and In Vivo. Chemistry & Biology 18: 833-838.
26. Madani F, Lindberg S, Langel U, Futaki S, Graslund A, (2011) Mechanisms of cellular uptake of cell-penetrating peptides. J Biophys 2011: 414729.
27. Thompson DB, Villasenor R, Dorr BM, Zerial M, Liu DR, (2012) Cellular uptake mechanisms and endosomal trafficking of supercharged proteins. Chem Biol 19: 831-843.
28. Dobson CM, (2003) Protein folding and disease: a view from the first Horizon Symposium. Nature Reviews Drug Discovery 2: 154-160.
29. Horwich A, (2002) Protein aggregation in disease: a role for folding intermediates forming specific multimeric interactions. Journal of Clinical Investigation 110: 1221-1232.
30. Xu J, Reumers J, Couceiro JR, De Smet F, Gallardo R, et al. (2011) Gain of function of mutant p53 by coaggregation with multiple tumor suppressors. Nature Chemical Biology 7: 285-295.
31. Lawrence MS, Phillips KJ, Liu DR, (2007) Supercharging proteins can impart unusual resilience. Journal of the American Chemical Society 129: 10110-10112.
32. Street AG, Mayo SL, (1999) Intrinsic beta-sheet propensities result from van der Waals interactions between side chains and the local backbone. Proceedings of the National Academy of Sciences of the United States of America 96: 9074-9076.
33. Loladze VV, Makhatadze GI, (2002) Removal of surface charge-charge interactions from ubiquitin leaves the protein folded and very stable. Protein Science 11: 174-177.
34. Makhatadze GI, Loladze VV, Ermolenko DN, Chen XF, Thomas ST, (2003) Contribution of surface salt bridges to protein stability: Guidelines for protein engineering. Journal of Molecular Biology 327: 1135-1148.
35. Horovitz A, Serrano L, Avron B, Bycroft M, Fersht AR, (1990) Strength and Cooperativity of Contributions of Surface Salt Bridges to Protein Stability. Journal of Molecular Biology 216: 1031-1044.
36. Tokuriki N, Stricher F, Schymkowitz J, Serrano L, Tawfik DS, (2007) The stability effects of protein mutations appear to be universally distributed. Journal of Molecular Biology 369: 1318-1332.
37. Leaver-Fay A, Tyka M, Lewis SM, Lange OF, Thompson J, et al. (2011) ROSETTA3: an object-oriented software suite for the simulation and design of macromolecules. Methods Enzymol 487: 545-574.
38. Das R, Baker D, (2008) Macromolecular modeling with rosetta. Annu Rev Biochem 77: 363-382.
39. Rohl CA, Strauss CEM, Misura KMS, Baker D (2004) Protein structure prediction using rosetta. Methods in Enzymology 383: 66-+.
40. Kuhlman B, Dantas G, Ireton GC, Varani G, Stoddard BL, et al. (2003) Design of a novel globular protein fold with atomic-level accuracy. Science 302: 1364-1368.
41. Herberhold H, Marchal S, Lange R, Scheyhing CH, Vogel RF, et al. (2003) Characterization of the pressure-induced intermediate and unfolded state of red-shifted green fluorescent protein- A Static and Kinetic FTIR, UV/VIS and Fluorescence Spectroscopy Study. Journal of Molecular Biology 330: 1153-1164.
42. Scheyhing CH, Meersman F, Ehrmann MA, Heremans K, Vogel RF, (2002) Temperature-pressure stability of green fluorescent protein: A Fourier transform infrared spectroscopy study. Biopolymers 65: 244-253.
43. Tsien RY, (1998) The green fluorescent protein. Annu Rev Biochem 67: 509-544.
44. Reid BG, Flynn GC, (1997) Chromophore formation in green fluorescent protein. Biochemistry 36: 6786-6791.
45. Jacak R, Leaver-Fay A, Kuhlman B, (2012) Computational protein design with explicit consideration of surface hydrophobic patches. Proteins-Structure Function and Bioinformatics 80: 825-838.
46. Li S, Bradley P (2013) Probing the role of interfacial waters in protein-DNA recognition using a hybrid implicit/explicit solvation model. Proteins.
47. Hirst SJ, Alexander N, McHaourab HS, Meiler J, (2011) RosettaEPR: an integrated tool for protein structure determination from sparse EPR data. J Struct Biol 173: 506-514.
48. Leaver-Fay A, O'Meara MJ, Tyka M, Jacak R, Song Y, et al. (2013) Scientific benchmarks for guiding macromolecular energy function improvement. Methods Enzymol 523: 109-143.
49. Liu Y, Kuhlman B, (2006) RosettaDesign server for protein design. Nucleic Acids Res 34: W235-238.
50. Lyskov S, Gray JJ, (2008) The RosettaDock server for local protein-protein docking. Nucleic Acids Research 36: W233-W238.
51. Sircar A, Kim ET, Gray JJ, (2009) RosettaAntibody: antibody variable region homology modeling server. Nucleic Acids Research 37: W474-W479.
52. Lyskov S, Chou FC,? Conchuir SO, Der BS, Drew K, et al. (2013) Serverification of Molecular Modeling Applications: the Rosetta Online Server that Includes Everyone (ROSIE). PLoS One.
53. Thompson DB, Cronican JJ, Liu DR, (2012) Engineering and identifying supercharged proteins for macromolecule delivery into mammalian cells. Methods in Enzymology 503: 293-319.
54. Pedelacq JD, Cabantous S, Tran T, Terwilliger TC, Waldo GS, (2006) Engineering and characterization of a superfolder green fluorescent protein. Nat Biotechnol 24: 79-88.
55. Sokalingam S, Raghunathan G, Soundrarajan N, Lee SG (2012) A Study on the Effect of Surface Lysine to Arginine Mutagenesis on Protein Stability and Structure Using Green Fluorescent Protein. PLoS One 7.
56. Mrabet NT, Vandenbroeck A, Vandenbrande I, Stanssens P, Laroche Y, et al. (1992) Arginine Residues as Stabilizing Elements in Proteins. Biochemistry 31: 2239-2253.
57. Borders CL, Broadwater JA, Bekeny PA, Salmon JE, Lee AS, et al. (1994) A Structural Role for Arginine in Proteins- Multiple Hydrogen-Bonds to Backbone Carbonyl Oxygens. Protein Science 3: 541-548.
58. Thompson D, Cronican J, Liu D, (2012) Engineering and identifying supercharged proteins for macromolecule delivery into mammalian cells. Methods in Enzymology 503: 293-319.
59. Gallivan JP, Dougherty DA, (1999) Cation-pi interactions in structural biology. Proceedings of the National Academy of Sciences of the United States of America 96: 9459-9464.
60. Strickler SS, Gribenko AV, Gribenko AV, Keiffer TR, Tomlinson J, et al. (2006) Protein stability and surface electrostatics: A charged relationship. Biochemistry 45: 2761-2766.
61. Takano K, Tsuchimori K, Yamagata Y, Yutani K, (2000) Contribution of salt bridges near the surface of a protein to the conformational stability. Biochemistry 39: 12375-12381.